Hybridization Promotes Asexual Reproduction in Caenorhabditis Nematodes. Caenorhabditis nouraguensis and Caenorhabditis becei

Although most unicellular organisms reproduce asexually, most multicellular eukaryotes are obligately sexual. This implies that there are strong barriers that prevent the origin or maintenance of asexuality arising from an obligately sexual ancestor. By studying rare asexual animal species we can gain a better understanding of the circumstances that facilitate their evolution from a sexual ancestor. Of the known asexual animal species, many originated by hybridization between two ancestral sexual species. The balance hypothesis predicts that genetic incompatibilities between the divergent genomes in hybrids can modify meiosis and facilitate asexual reproduction, but there are few instances where this has been shown. Here we report that hybridizing two sexual Caenorhabditis nematode species (C. nouraguensis females and C. becei males) alters the normal inheritance of the maternal and paternal genomes during the formation of hybrid zygotes. Most offspring of this interspecies cross die during embryogenesis, exhibiting inheritance of a diploid C. nouraguensis maternal genome and incomplete inheritance of C. becei paternal DNA. However, a small fraction of offspring develop into viable adults that can be either fertile or sterile. Fertile offspring are produced asexually by sperm-dependent parthenogenesis (also called gynogenesis or pseudogamy); these progeny inherit a diploid maternal genome but fail to inherit a paternal genome. Sterile offspring are hybrids that inherit both a diploid maternal genome and a haploid paternal genome. Whole-genome sequencing of individual viable worms shows that diploid maternal inheritance in both fertile and sterile offspring results from an altered meiosis in C. nouraguensis oocytes and the inheritance of two randomly selected homologous chromatids. We hypothesize that hybrid incompatibility between C. nouraguensis and C. becei modifies maternal and paternal genome inheritance and indirectly induces gynogenetic reproduction. This system can be used to dissect the molecular mechanisms by which hybrid incompatibilities can facilitate the emergence of asexual reproduction.

尽管多数单细胞生物以无性方式繁殖，但绝大多数多细胞真核生物均为专性有性生殖。这意味着存在强进化障碍，阻碍了从专性有性祖先演化出无性生殖的起源与维持。通过研究珍稀的无性生殖动物类群，我们能够更深入地理解促成其从有性祖先演化而来的具体情境。在目前已发现的无性生殖动物物种中，多数起源于两个祖先有性物种间的杂交事件。平衡假说提出：杂交物种中分化基因组间的遗传不相容性，可改变减数分裂过程并促进无性生殖的形成，但目前鲜有该假说的实证案例。本研究通过杂交两种有性生殖的杆状线虫属（Caenorhabditis）物种——诺拉格杆状线虫（C. nouraguensis）雌性个体与贝氏杆状线虫（C. becei）雄性个体，发现杂交合子形成过程中，亲本基因组的正常遗传模式发生改变。该种间杂交的多数子代在胚胎发育阶段死亡，其基因组表现为仅继承二倍体的诺拉格杆状线虫母本基因组，且贝氏杆状线虫的父本DNA遗传不完全。但极少数子代可发育为可存活的成虫，这些个体可分为可育与不育两类。可育子代通过依赖精子的孤雌生殖（又称雌核发育或假受精）以无性方式产生：此类子代继承二倍体母本基因组，但未获得父本基因组。不育子代则为杂交个体，同时继承了二倍体母本基因组与单倍体父本基因组。对单个存活线虫的全基因组测序结果显示：可育与不育子代的二倍体母本遗传模式，均源于诺拉格杆状线虫卵母细胞的减数分裂异常，且随机继承了两条同源染色单体。我们提出假说：诺拉格杆状线虫与贝氏杆状线虫间的杂交不相容性，会改变亲本基因组的遗传模式，并间接诱导雌核发育生殖。该实验体系可用于解析杂交不相容性如何推动无性生殖起源的分子机制。